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Gait & Posture 23 (2006) 348354

www.elsevier.com/locate/gaitpost

Postural strategy changes with fatigue of the lumbar extensor muscles


Erin L. Wilson a, Michael L. Madigan a,*, Bradley S. Davidson a, Maury A. Nussbaum b
a
Department of Engineering Science and Mechanics, Virginia Polytechnic Institute and State University, Mail Code 0219, Blacksburg, VA 24061, USA
b
Grado Department of Industrial and Systems Engineering, Virginia Polytechnic Institute and State University,
250 Durham Hall (0118), Blacksburg, VA 24061, USA
Received 1 February 2005; accepted 15 April 2005

Abstract

The purpose of this study was to investigate the effect of lumbar extensor fatigue on postural strategy in response to a balance perturbation.
Anteriorly-directed force perturbations were applied to the upper back with a padded pendulum and attempted to challenge the postural
control system without eliciting a stepping response. In three separate sessions, subjects were perturbed both before and after a fatiguing
protocol that induced lumbar extensor fatigue to one of three different fatigue levels. Postural strategy was quantified using center of pressure
position along with joint angles and joint torques for the ankle, knee, hip, and low back joints. Results showed both proactive and reactive
changes in postural strategy. Proactive changes involved a slight anterior lean prior to the perturbation, and reactive changes were consistent
with a shift toward more of a hip strategy with fatigue. In addition, results suggested that subjects classified as moving mostly at the hip prior to
fatigue were more affected by fatigue compared to subjects classified as moving roughly equal amounts at the ankle and hip prior to fatigue.
Increasing fatigue level exaggerated some, but not all, of the changes in postural strategy with fatigue. These findings illustrate that
neuromuscular fatigue can influence postural strategy in response to a balance perturbation.
# 2005 Elsevier B.V. All rights reserved.

Keywords: Postural strategy; Fatigue; Perturbation; Balance

1. Introduction Neuromuscular fatigue is another intrinsic factor that


may affect postural strategy, but to our knowledge no studies
Movements used to maintain standing balance in the have investigated fatigue in this regard. Fatigue has been
sagittal plane following a postural perturbation have been shown to increase postural sway during quiet standing [14
described as a hip strategy, ankle strategy, or a combination 20]. Increases in postural sway have, in turn, been associated
of the two [1,2]. Numerous extrinsic and intrinsic factors with changes in postural strategy [21,22]. For example, Kuo
affect, which of these postural strategies are typically et al. (1998) administered the Sensory Organization Test to
employed. Extrinsic factors include support surface size [3], healthy subjects and observed an increase in postural sway
perturbation magnitude [4], perturbation direction [5], and along with an increase in hip strategy when somatosensory
body position prior to the perturbation [6]. These studies information was disrupted. Although this study did not focus
suggest that postural strategy is affected by the biomecha- on fatigue, it demonstrates potential effects of a change in
nical demands associated with maintaining balance. postural strategy on postural sway. Similarly, the docu-
Intrinsic factors include fear of falling [7], expectation of mented increase in postural sway during quiet standing with
perturbation characteristics [8], quality of somatosensory fatigue may result from a change in postural strategy. If
and vestibular feedback [9], Parkinsons disease [10], aging fatigue induces changes in postural strategy during quiet
[11], low back pain [12], and respiration [13]. standing, it seems logical that similar changes in postural
strategy will occur in response to a postural perturbation.
The purpose of this study was to investigate the effect of
* Corresponding author. Tel.: +1 540 231 1215; fax: +1 540 231 4574. lumbar extensor fatigue on postural strategy in response to a
E-mail address: mlmadigan@vt.edu (M.L. Madigan). balance perturbation. The effect of lumbar extensor fatigue

0966-6362/$ see front matter # 2005 Elsevier B.V. All rights reserved.
doi:10.1016/j.gaitpost.2005.04.005
E.L. Wilson et al. / Gait & Posture 23 (2006) 348354 349

level was also investigated to determine if increasing levels


of fatigue have increasing effects on postural strategy.
Understanding any changes in postural strategy with fatigue
will further our basic understanding of postural control, and
potentially contribute to the development of interventions
aimed at mitigating the effect of fatigue on balance. One
application of such an intervention would be in the
construction industry where fatigue-related loss of balance
may contribute to over 300 deaths/year from falls from
heights [23]. Lumbar extensor fatigue was investigated
because it is common during many occupational lifting tasks
[24], and muscle fatigue in general has been shown to
increase the risk of falling from heights [25].

2. Methods

Twelve physically active males (2022 years of age) Fig. 1. Experimental set-up for applying postural perturbations. Subjects
participated in the experiment. Mean (S.D.) participant were perturbed by releasing the pendulum after pulling it back a fixed
distance from the subject.
height and mass were 173.7(6.4) cm and 70.2(6.6) kg,
respectively. None of the participants reported any history of
low back pain or injury, and all provided informed consent in
accordance with the Virginia Tech Institutional Review postural control system without eliciting a stepping
Board before participation. response. Using this method, the perturbation peak force
Participants completed three experimental sessions with was 177(21) N, and the perturbation impulse was
12 weeks between sessions. Each session consisted of four 13.2(1.3) N s. Perturbations were applied following a
stages: warm-up, unfatigued balance perturbations, fati- random delay (015 s) from the beginning of each data
guing protocol, and a fatigued balance perturbation. For collection to reduce participant anticipation.
warm-up, participants completed two cycles of the follow- In each of the three experimental sessions, the lumbar
ing activities: jogging at 2.0 km/h on a treadmill for 21/ extensor muscles were fatigued to either 86, 73, or 60% of
2 min, stretching the lumbar extensors, and performing five their unfatigued MVC. A balanced Latin square was used to
back extensions on a 458 Roman chair (New York Barbell, determine the order of presentation of the three fatigue
Elmira, NY). Following warm-up, the unfatigued isometric levels. The fatiguing protocol consisted of multiple sets of
maximum voluntary contraction (MVC) moment of the back extensions and intermittent MVCs performed on the
lumbar extensors was measured at the level of L3. Roman chair (see [15] for more details). Investigators
Participants were positioned in the Roman chair, attached attempted to fatigue participants such that their MVC
to a load cell (Cooper Instruments and Systems, Warrenton, moment decreased linearly over the duration of the fatiguing
VA) at the mid-sternum via a modified construction harness, protocol and achieved the desired fatigue level over 14 min.
and instructed to extend at the back as hard as possible. In The fatigue levels actually achieved were 82(5), 70(5), and
this position the lumbar flexion angle was approximately 62(6)% MVC, which were significantly different from each
458. Participants performed three isometric MVCs separated other ( p < 0.001). Prior to performing the back extensions,
by 1 min of rest; the largest of the three was recorded as the participants were instructed to keep their feet flat on the base
unfatigued MVC value. of the Roman chair and move through approximately 458
Three unfatigued balance perturbations were performed range of motion from 08 lumbar flexion to maximum flexion.
following the warm-up. Prior to the perturbation, partici- Participants performed one set of back extensions every
pants were instructed to stand quietly on a force platform minute of the fatiguing protocol and an isometric back
without shoes, with their eyes closed, feet together, and arms extension MVC every 2 min. MVCs were performed 10 s
resting at their side (Fig. 1). Participants were also told that if after completing the prior set of back extensions. A digital
they stepped to regain their balance, another collection metronome set at 30 beats/min was used to ensure all
would be taken. (Two perturbations were repeated due to participants performed the extensions at a similar rate. The
stepping.) Perturbations consisted of an anteriorly-directed number of repetitions in each set was systematically
force applied in the mid-sagittal plane at the level of the adjusted based upon a comparison of each measured
inferior margin of the scapulae, and were applied using a MVC moment to the target moment [15]. If participants
padded pendulum that was pulled a fixed distance away from were not at or below the desired fatigue level at the end of the
the subject and released. These perturbations were designed fatiguing protocol, 2 min were added with additional
to mimic a bump to the upper back and challenge the repetitions according to the same method. This process
350 E.L. Wilson et al. / Gait & Posture 23 (2006) 348354

was continued until the MVC was below the desired fatigue preparatory activity prior to the perturbation, and the second
level. used dependent measures quantifying strategy during
Within 20 s after completing the fatiguing protocol, one recovery from the perturbation. Data from all four joints
fatigued balance perturbation was performed in an identical were included in each MANOVA with the independent
manner as the unfatigued perturbations. Only one fatigued variables being fatigue (two levels: unfatigued and fatigued)
perturbation was performed to minimize recovery from and fatigue level (three levels: 86% MVC, 73% MVC, and
fatigue. 60% MVC). A significant main effect was followed by a
During each trial, the perturbation force was sampled at two-way repeated measures analysis of variance (ANOVA)
1000 Hz from a load cell mounted inline with the pendulum for each dependent variable. Correlation analysis was
and subsequently low-pass filtered at 25 Hz (fourth order performed to determine the strength of any relationship
zero-phase-lag Butterworth filter). Triaxial ground reaction between measures quantifying preparatory activity prior to
forces and moments were low-pass filtered with a 500 Hz the perturbation and measures quantifying strategy during
anti-aliasing hardware filter, amplified, and sampled at recovery from the perturbation. A significance level of
1000 Hz with a Bertec K20102 type 9090-15 force platform p  0.05 was used for all tests.
(Bertec Corp., Columbus, OH). These data were subse- To determine if perturbations were consistent across
quently low-pass filtered at 10 Hz (fourth order zero-phase- fatigue states, a two-way repeated measures MANOVA was
lag Butterworth filter) and transformed to obtain ground also used to determine if perturbation peak force and
reaction forces (GRF) and center of pressure (COP) data impulse were affected by fatigue and fatigue level.
[26]. Body position was sampled at 50 Hz using a Vicon 460 Perturbation peak force decreased 4.3(6.4)% with fatigue
motion analysis system (Vicon Motion Systems Inc., Lake ( p = 0.013), and there was no effect of fatigue level or
Forest, CA). Markers were placed on both sides of the body fatigue  fatigue level interaction for either parameter.
at the acromion, iliac crest, greater trochanter, lateral
femoral epicondyle, lateral malleolus, calcaneus, and head
of the fifth metatarsal. Marker position data was low pass 3. Results
filtered at 7 Hz (fourth order zero-phase-lag Butterworth
filter) and averaged across both sides of the body to create a Although a fair amount of inter-subject variability was
sagittal plane representation of the body with five segments observed, a general pattern of joint angles and torques
including the feet, shanks, thighs, pelvis, and trunk (defined emerged across all subjects during unfatigued trials (Fig. 2).
by the iliac crest and shoulder). Using these five segments, Prior to the perturbation, initial joint angles were
joint angles were calculated for the ankle, knee, hip, and approximately zero (i.e. anatomical position). Initial ankle
low back joints (the low back joint is defined as the angle and knee torques were plantar flexor and flexor dominant,
between the trunk and pelvis segments). Joint torques were respectively, while the initial hip and low back torques were
estimated using an inverse dynamics analysis with a model more variable. Following the perturbation, the initial
of the body consisting of five rigid segments connected by response was a flexor torque at the knee and extensor
frictionless pin joints. The mass and inertial characteristics torques at the hip and low back. These torques were followed
of the segments were defined using an anthropometric model 1030 ms later by a plantar flexor torque at the ankle and
[27]. flexion at the knee, hip, and low back. Ankle plantar flexion
Three dependent measures were calculated to quantify began 2080 ms after the ankle torque. The entire recovery
preparatory activity prior to the perturbation including initial duration was approximately 2 s. The timing of joint angles
joint angles, initial joint torques, and initial COP position and torques were consistent within the unfatigued trials and
relative to the ankle. These initial values were calculated as were not affected by fatigue, fatigue level, or their
the mean over the time interval from 540 to 40 ms prior to interaction.
the perturbation. Four dependent measures were calculated Fatigued recoveries exhibited the same general pattern of
to quantify postural strategy during recovery from perturba- joint angles and torques as in the unfatigued recoveries, but
tions including peak joint angles, time to peak joint angles, some specific differences existed. Prior to the perturbation,
peak joint torques, and time to peak joint torques. Because initial joint angles did not change with fatigue ( p = 0.441),
initial joint torques prior to the perturbation were affected by but the COP position was 1.1(1.7) cm more anterior from the
fatigue (see Section 3), peak joint torques relative to their ankle compared to unfatigued trials ( p = 0.012). The
initial values were used rather than absolute torques. Only anterior displacement of the COP during static stance
data from the third unfatigued balance perturbation was used suggests increased plantar flexor activity and necessitates a
in the analysis because of possible learning effects within the forward lean (the magnitude of which was evidently too
three unfatigued perturbations [28]. small to be detected in joint angle measurements). As a
To determine the effect of fatigue and fatigue level on result of this slight forward lean when fatigued, initial joint
postural strategy, two separate two-way repeated measures torques at all four joints changed with fatigue; offsets were
multivariate analysis of variance (MANOVA) were used. in the direction of the maximum torque for each joint. More
The first MANOVA used dependent measures quantifying specifically, initial ankle torque shifted 7.1(1.1) N m in the
E.L. Wilson et al. / Gait & Posture 23 (2006) 348354 351

plantar flexion torque 3.2(2.1) N m ( p = 0.002), did not


affect peak knee torque ( p = 0.310), increased peak hip
extensor torque 10.2(1.2) N m ( p = 0.044), and increased
peak low back extension torque 9.4(0.8) N m ( p = 0.013).
Fatigue level also had an effect on several dependent
measures. Increasing fatigue level from 86% MVC to 60%
MVC increased peak low back flexion 4.6(7.0)8 ( p = 0.049),
decreased peak ankle plantar flexor torque 5.8(6.4) N m
( p = 0.030), decreased peak knee flexor torque 6.8(7.0) N m
( p = 0.005), and decreased hip extensor torque 3.8(8.3) N m
( p = 0.034). Fatigue level had no effect on peak low back
torque ( p = 0.376), and there were no fatigue  fatigue level
interactions for peak joint angles or torques.
Correlations between initial COP position and peak joint
angles/torques revealed minimal covariance between these
variables except for one peak torque value. Peak ankle
torque exhibited a small but statistically significant
correlation with initial COP position (r2 = 0.19; p < 0.05).
The coefficient of determination for all other correlations
were r2 = 0.01(0.01), and none were statistically significant.
Although all subjects exhibited the same general
recovery patterns that are best described as a mixed strategy,
subjects could be classified into two groups based on the
amount of movement at the hip and ankle during unfatigued
recoveries (Fig. 4). Through visual inspection of the
unfatigued data, eight of the twelve subjects were found
to move predominantly at the hip and low back and were
classified as using more of a hip strategy. The remaining four
subjects showed similar amounts of movement at the ankle,
hip, and low back, and were classified as using a true mixed
strategy. The effects of fatigue on postural strategy were
more pronounced in the hip strategy group. For the hip
strategy group, fatigue increased peak ankle plantar flexion
2.4(3.4)8, increased hip flexion 5.2(8.0)8, and increased low
back flexion 8.4(11.0)8. For the mixed strategy group,
fatigue increased peak ankle plantar flexion 2.9(2.8)8,
Fig. 2. Representative joint angles and torques during recovery from an
increased hip flexion 1.9(2.1)8, and increased low back
unfatigued postural perturbation. Positive values indicate extension move- flexion 3.5(3.9)8, respectively.
ment (relative to anatomical position) and extensor torque. The perturbation
time is indicated with a dotted line. The plots show the general patterns
observed from the subjects. 4. Discussion

plantar flexor direction ( p = 0.006), initial knee torque Neuromuscular fatigue has been shown to increase
shifted 4.8(3.8) N m in the flexion direction ( p = 0.010), postural sway during quiet standing [1420]. The increase in
initial hip torque shifted 6.5(1.7) N m in the extensor sway may, in part, be the result of a change in postural
direction ( p < 0.001), and initial low back torque shifted control strategy. The purpose of the present study was to
6.1(1.4) N m in the extensor direction ( p = 0.001). There investigate the effects of lumbar extensor fatigue and fatigue
were no fatigue level effects or fatigue  fatigue level level on postural strategy in response to a balance
interactions for initial COP position, initial joint angles, or perturbation. Our results showed both proactive and reactive
initial joint torques. changes in postural strategy with fatigue. For the purposes of
Both peak joint angles and torques after the perturbation this report, proactive changes are operationally defined to be
were affected by fatigue (Fig. 3) and fatigue level. Fatigue changes occurring prior to the perturbation, and reactive
increased peak ankle plantar flexion 2.5(0.5)8 ( p = 0.002), changes are the changes occurring after the perturbation.
did not affect peak knee ( p = 0.170) or hip ( p = 0.062) Proactive changes involved adopting a slight forward lean
angles, and increased peak low back flexion 6.3(1.6)8 prior to the perturbation as evidenced by an anterior shift in
( p = 0.021). In addition, fatigue decreased peak ankle the COP, while reactive changes indicate a shift toward hip
352 E.L. Wilson et al. / Gait & Posture 23 (2006) 348354

Fig. 3. Representative joint angle and joint torque data during unfatigued and fatigued postural recoveries. Positive values indicate extension movement
(relative to anatomical position) and extensor torque. Joint angle plots show increases in peak ankle plantar flexion and peak low back flexion with fatigue. Joint
torque plots show initial torque offsets and increases in ankle, hip, and low back extensor torques with fatigue. Figures in the middle illustrate differences in
unfatigued and fatigue recoveries at the instant of maximum hip flexion.

strategy. Increasing fatigue level exaggerated some, but not with fatigue, mechanics necessitates at least a slight forward
all, of these changes. Interestingly, the changes were not lean due to the COP shift.
limited to the fatigue location. In both unfatigued and fatigued recoveries, subjects
The proactive change in postural strategy involved a generally used a mixed strategy; however, reactive changes
1.1(1.7) cm anterior displacement of the COP prior to the with fatigue showed a shift toward more of a hip strategy.
perturbation. Although a post hoc analysis of the angle Changes in peak torques indicated a clear shift toward a hip
between the ankle and whole-body center-of-mass (COM) strategy, as evidenced by a 3.2 N m decrease in plantar flexor
prior to the perturbation did not show a significant increase torque and a 10.2 N m increase in hip extensor torque. The
2.58 increase in peak ankle plantar flexion is consistent with
this shift, since the hip strategy involves simultaneous hip
flexion and ankle plantar flexion. Although the increase in
peak hip flexion was only a trend ( p = 0.062), peak low back
flexion increased 6.38, which provides a similar benefit to
recovery as hip flexion by attempting to reduce the body
moment of inertia about the ankle [4]. Taken together, we
feel that these results indicate a shift toward more of a hip
strategy with lumbar extensor fatigue. It was also interesting
to note that peak low back extension torque increased
9.4 N m despite subjects being fatigued.
According to past studies [5], the change in reactive
postural strategy could be partially attributed to the forward
lean. However, three arguments suggest otherwise. First, low
correlations between initial COP position and peak joint
angles/torques indicate a weak relationship between these
measures. Second, a follow-up analysis was performed by
Fig. 4. Differences in peak joint angles and torques between the hip and repeating our statistical analysis on a subset of participants
mixed group. Both line plots show a greater affect of fatigue on the hip whose change in initial COP with fatigue was less than the
group as compared to the mixed group. The stick figures show the general overall mean of 1.1 cm (seven participants). This subset of
patterns of movement for both groups. The dotted figure is the initial
(anatomical) position while the solid figure is the maximum displacement participants showed no change in initial COP position with
from the initial position following the perturbation. Standard deviation bars fatigue ( p = 0.286), and significant changes in reactive
were omitted for clarity, but these data are available from the authors. measures with fatigue that were similar to the overall
E.L. Wilson et al. / Gait & Posture 23 (2006) 348354 353

analysis: peak ankle angle increased ( p = 0.046), peak hip level would exaggerate the effect of fatigue. This was the
extensor torque increased ( p = 0.031), and peak low back case with peak low back flexion, peak ankle plantar flexor
extensor torque increased ( p = 0.012). Third, comparing torque, and peak knee flexor torque. The decrease in ankle
lean angles in the present study with those of another study movement and increase in low back movement is consistent
suggest that the leans here were too small to elicit a change with more of a hip strategy. This was not the case, however,
in recovery strategy. Horak and Moore [6] reported that a hip with peak hip extensor torque. Fatigue increased peak hip
strategy is favored when pre-leaning in the same direction as extensor torque, but increasing fatigue level from 86% MVC
an induced sway. However, this shift in strategy was only to 60% MVC decreased peak hip extensor torque an average
found when subjects assumed a maximum forward lean (an of 3.85 N m. In other words, increasing fatigue level
average 6.098 from normal standing posture). No change in decreased the effect of fatigue on the hip. This may reflect
strategy was found when subjects assumed a half-maximum a continuous adaptation of postural strategy with increasing
forward lean (an average 3.018). The average forward lean in level of fatigue. It is interesting to note that the only joint that
our study was 0.258, which is much smaller than either of the did not exhibit a change in peak torque with increasing level
leans reported. For these reasons, we do not attribute the of fatigue was the joint that was fatigued.
reactive changes in postural strategy to the forward lean It appears that even in the absence of any influencing
prior to the perturbation. factors, differences in preferred postural strategies exist
Reasons why a shift toward more of a hip strategy and an between individuals. Subtle differences in peak joint angles
increase in forward lean were observed with lumbar extensor during unfatigued perturbations allowed subjects to be
fatigue remain to be explained. In regards to the forward categorized into two strategy groups (Fig. 4). Horak and
lean, we feel it is unlikely that lumbar extensor fatigue Nashner [30] similarly reported that some subjects
directly elicits an increase in plantar flexor activity without employed pure ankle or hip strategies while others used a
any other biomechanical or physiological explanation. One mixed strategy even after 2040 trials. In the present study,
reason for the lean, independent of fatigue, may be that there was a tendency for subjects using more of a hip
subjects unintentionally leaned forward with repeated strategy when unfatigued to be more heavily influenced by
exposure to the balance perturbation. Such a habituation fatigue compared to subjects using a mixed strategy when
has been reported [8]. This habituation, however, seems to unfatigued. These data suggest that an individuals preferred
occur mostly in the first few perturbations [28], and we postural strategy may dictate how much they are affected by
allowed 3 unfatigued perturbations to allow for habituation certain influencing factors. Postural strategy may be related
prior to fatiguing subjects. Also, there was no difference in to postural performance and the ability to prevent a fall
COP initial position between the second and third after a perturbation, but future work is needed to establish
unfatigued perturbations ( p = 0.907), suggesting that habi- this relationship.
tuation had already occurred. Another potential reason is Several methodological issues warrant discussion. First,
related to motor control. Lumbar extensor fatigue has been one may question whether the measured changes in postural
associated with an increase in antagonist muscle activity in strategy were due to fatigue or the 4.3% decrease in
the rectus abdominus muscle (RA) [29]. We analyzed perturbation amplitude. Runge et al. [4] reported greater
muscle activity data from five subjects that was collected for shifts toward hip strategy with increasing perturbation
a separate study and found baseline RA activity increased an amplitude (i.e. increases in platform velocity). Our
average of 54% with lumbar extensor fatigue prior to the perturbation amplitude decreased with fatigue by an average
perturbation ( p = 0.033). Forward leaning has also been of 8 N (decrease in perturbation force). Because of this, we
associated with an increase in RA activity [6]. The increase feel that if perturbation amplitude did not decrease with
in RA activity prior to the perturbation may be a part of a fatigue, the measured shift toward hip strategy would have
subtle adaptation in postural control that displaced the COP been larger. The reason for this change in perturbation
forward. Interestingly, Runge et al. [4] reported higher hip amplitude with fatigue is beyond the scope of this study, but
torques (i.e. more of a hip strategy) during perturbation may be related to a decrease in trunk stiffness with lumbar
recoveries that involved elevated RA activity (although their extensor fatigue. Second, one may question whether the
perturbation method involved a moving platform rather than measured changes in reactive strategy were due to changes
a trunk impulse). Thus, an increase in RA activity from in initial COP position. While we cannot rule this out, we
lumbar extensor fatigue has the potential to contribute to feel the low correlations between the initial COP position
both the forward lean prior to the perturbation and the shift and reactive measures, along with the result from our follow-
toward more of a hip strategy in response to the perturbation. up analysis (individuals who had no change in initial COP
The last potential explanation is attractive because it links position still exhibited a shift toward hip strategy with
the effects of lumbar extensor fatigue with both the proactive fatigue), provide strong evidence supporting the fact that
and reactive changes in postural strategy observed. almost all of the reactive changes were not due to changes in
It seems reasonable that increasing levels of fatigue initial COP position. Third, all learning affects were
would lead to larger influences on postural strategy. Such a assumed to have happened during the unfatigued balance
dose-response relationship implies that increasing fatigue perturbations. Fourth, we acknowledge that our relatively
354 E.L. Wilson et al. / Gait & Posture 23 (2006) 348354

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